Neural Computations Mediating One-Shot Learning in the Human Brain

Sang Wan Lee, John P O’Doherty and Shinsuke Shimojo

PLOS Biology, 2015, vol. 13, issue 4, 1-36

Abstract: Incremental learning, in which new knowledge is acquired gradually through trial and error, can be distinguished from one-shot learning, in which the brain learns rapidly from only a single pairing of a stimulus and a consequence. Very little is known about how the brain transitions between these two fundamentally different forms of learning. Here we test a computational hypothesis that uncertainty about the causal relationship between a stimulus and an outcome induces rapid changes in the rate of learning, which in turn mediates the transition between incremental and one-shot learning. By using a novel behavioral task in combination with functional magnetic resonance imaging (fMRI) data from human volunteers, we found evidence implicating the ventrolateral prefrontal cortex and hippocampus in this process. The hippocampus was selectively “switched” on when one-shot learning was predicted to occur, while the ventrolateral prefrontal cortex was found to encode uncertainty about the causal association, exhibiting increased coupling with the hippocampus for high-learning rates, suggesting this region may act as a “switch,” turning on and off one-shot learning as required.A combination of neuroimaging and computational modeling suggests that a part of ventrolateral prefrontal cortex, in cooperation with the hippocampus, is responsible for switching between incremental and one-shot strategies for learning about causal relationships. Read the Synopsis.Author Summary: There are at least two distinct learning strategies for identifying the relationship between a cause and its consequence: (1) incremental learning, in which we gradually acquire knowledge through trial and error, and (2) one-shot learning, in which we rapidly learn from only a single pairing of a potential cause and a consequence. Little is known about how the brain switches between these two forms of learning. In this study, we provide evidence that the amount of uncertainty about the relationship between cause and consequence mediates the transition between incremental and one-shot learning. Specifically, the more uncertainty there is about the causal relationship, the higher the learning rate that is assigned to that stimulus. By imaging the brain while participants were performing the learning task, we also found that uncertainty about the causal association is encoded in the ventrolateral prefrontal cortex and that the degree of coupling between this region and the hippocampus increases during one-shot learning. We speculate that this prefrontal region may act as a “switch,” turning on and off one-shot learning as required.

Date: 2015
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Persistent link: https://EconPapers.repec.org/RePEc:plo:pbio00:1002137

DOI: 10.1371/journal.pbio.1002137

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